Repercussions of the Emergency neurological life support on scientific literature: a bibliometric study

Background  In 2012, the Neurocritical Care Society launched a compilation of protocols regarding the core issues that should be addressed within the first hours of neurological emergencies – the Emergency neurological life support (ENLS). Objective  We aim to evaluate this repercussion through a bibliometric analysis. Methods  We searched Scopus on October 2022 for articles mentioning ENLS. The following variables were obtained: number of citations; number of citations per year; number of publications per year; year of publication; research type; research subtype; country of corresponding author and its income category and world region; journal of publication and its 5-year impact factor (IF); and section where ENLS appeared. Results  After applying eligibility criteria, we retrieved 421 articles, published from 2012 to 2022. The mean number of citations per article was 17.46 (95% Confidence Interval (CI) = 8.20–26.72), while the mean number of citations per year per article was 4.05 (95% CI = 2.50–5.61). The mean destiny journal 5-year IF was 5.141 (95% CI = 4.189–6.093). The majority of articles were secondary research (57.48%; n  = 242/421) of which most were narrative reviews (71.90%; n  = 174/242). High-Income countries were the most prominent (80.05%; n  = 337/421 articles). There were no papers from low-income countries. There were no trials or systematic reviews from middle-income countries. Conclusion  Although still low, the number of publications mentioning ENLS is increasing. Articles were mainly published in journals of intensive care medicine, neurology, neurosurgery, and emergency medicine. Most articles were published by authors from high-income countries. The majority of papers were secondary research, with narrative review as the most frequent subtype.


INTRODUCTION
In 2012, the first edition of Emergency neurological life support (ENLS) protocols was published in Neurocritical Care, the official journal of the Neurocritical Care Society. 1 They were launched as a compilation of the core issues that should be addressed within the first hours of neurological emergencies, as recommended by experts and available evidence.Analogous to the Advanced Cardiovascular Life Support (ACLS) and Advanced Trauma Life Support (ATLS), the ENLS aims to standardize the initial approach to neurological emergencies. 2,35][6][7] There is no consensus on how to perform this kind of study, where a high number of different variables may be assessed, depending on the purpose.For instance, relying on the number of articles, citations, and derived metrics allows for the quantification of the most prominent journals, countries, and research types in a specific field.Recently, several bibliometric analyses have been published in the fields of neurology, 8,9 neurosurgery, 10,11 and neurocritical care. 12nfortunately, the ENLS is relatively recent and is not as widespread as the ACLS and ATLS.However, it is mentioned by several recent guidelines within neurocritical care research, [13][14][15] demonstrating interest in standardized and systematic approaches to critically ill neurological patients.We are unaware of studies that assessed the repercussions of the ENLS in the scientific literature.Therefore, we aim to evaluate such impact through a bibliometric analysis.

Search strategy
We searched Elsevier's Scopus on October 19 th , 2022 for articles mentioning ENLS in any part of the manuscript (title, abstract, keywords, text, or references).The exact search string is shown in Supplementary Material (https://www.arquivosdeneuropsiquiatria.org/wp-content/uploads/2023/10/ANP-2023.0104-Supplementary-Material.docx).Documents were excluded if they did not mention ENLS in any of these parts.Non-English studies, book chapters, conference abstracts, symposiums, discussion panels, erratum articles, as well as articles that could not have their full texts retrieved were also excluded.

Bibliometric analysis
The full text of all included articles was analyzed.The following variables were obtained from each article: number of citations; number of citations per year; number of publications per year; year of publication; research type; research subtype; country of corresponding author and its income category and world region; journal of publication and its 5-year impact factor (IF); and local of appearance of ENLS (title, abstract, keywords, text, or references).The number of citations per year was not retrieved from articles published in 2022.Research types were classified as Primary,

Statistical analysis
We used SPSS version 23.0 for Windows for statistical analysis.We used Prism Graphpad for creating charts.For continuous variables, we obtained the mean, 95% confidence interval (95%CI), and percentiles 25th, 50th, and 75th.Continuous variables presented an asymmetrical distribution (p < 0.001 on Kolmogorov-Smirnov test).Correlations were determined using Spearman rank correlation.We used the Mann-Whitney and Kruskal-Wallis tests for comparison of two means and three or more means, respectively.Pairwise post-hoc comparisons were performed after Kruskal-Wallis test.The level of significance was set at 5%.

General results
After applying eligibility criteria to the 618 retrieved documents, a total of 429 articles were included.Of these, we could not obtain the full texts of 8 articles.The region with the highest number of papers was North America (57.96%;N ¼ 244/421 articles).High-income coun-tries were the most prolific (80.05%;N ¼ 337/421 articles).There were no papers from low-income countries.Articles published by high-income countries had a higher mean number of citations and a higher mean number of citations per year than those published by middle-income countries (►Figures 3A and 3B).Conversely, there was no difference in the mean 5-year IF between income categories (►Figure 3C).Emergency neurological life support bibliometrics Ramos et al. 5 All of the ten most cited papers were published by authors from high-income countries.

Research type and subtype
The research types and subtypes of papers mentioning ENLS are detailed in ►Table 4. The most frequent research type was secondary research (57.48%;N ¼ 242/421 articles), followed by primary research (30.64%;N ¼ 129/421 articles).Among primary research articles, the research subtype with the greatest number of articles was Observational (92.25%;N ¼ 119/129).Among secondary research, in turn, the most common research subtype was Narrative Review (71.90%;N ¼ 174/242).Primary and secondary research were the study types of three and seven articles, respectively, of the ten most cited.There were no trials or systematic reviews from middle-income countries.

ENLS occurrences and ENLS protocols
ENLS appeared more often in the References section, followed by the Text section (►Figure 4).A total of

DISCUSSION
In this bibliometric study, we considered that the number of publications mentioning ENLS is low, with the majority of articles mentioning it only in the references section.However, this repercussion is increasing, demonstrating a growing interest in this subject (►Figure 1).Articles were mainly published in journals of intensive care medicine, neurology, neurosurgery, and emergency medicine.The majority of articles -including the most prominent -were published by authors from high-income countries.The majority of papers were secondary research, with narrative review as the most frequent subtype.
Neurocritical Care is the official journal of the Neurocritical Care Society, which is responsible for publishing ENLS protocols and other ENLS official publications. 1Our study demonstrated that this was the journal with the   Emergency neurological life support bibliometrics Ramos et al. 7 greatest number of articles mentioning ENLS (►Table 2), even when not considering ENLS official publications.In addition, we did not find a correlation between destiny journal 5-year IF and the number of publications (►Figure 2).In fact, journals related to a specific field tend to have a lower IF than general medicine journals. 16It does not mean, however, that these journals are less important.Actually, very specific journals -such as Neurocritical Careattract more frequently the attention of a relatively small number of readers (i.e., subspecialists) in comparison with more general journals.Also, IF varies widely across specialties, precluding generalized comparisons.For example, while the greatest IF of a neurosurgical journal is 5.526, a total of 17 cardiology journals and 31 oncology journals have an IF greater than 10 (data retrieved from https://jcr.clarivate.com/jcr/home).
In our study, high-income countries were the most prolific and the USA was the most prominent country (►Table 3).In addition, studies from high-income countries had a higher mean number of citations per article and a higher mean number of citations per year per article than studies from middle-income countries (►Figures 3A and 3B).Several prior bibliometric analyses of neurology and neurosurgery topics also showed that the USA was, by far, the most prominent country. 9,10,12The majority of papers mentioning ENLS were secondary research and a great portion were narrative reviews, which have a shallow level of evidence.Among primary research papers, we identified only 10 interventional -all of them from high-income countries (►Table 4).Actually, conducting original research in neurocritical care is challenging, especially interventional studies.It requires specialized training as well as specific resources to provide high-quality care, which are often scarce in developing countries. 17,18he "first hour" of neurological emergencies is critical, since a fast workup may significantly improve patients' outcomes.For instance, the recognition of ventilatory distress in patients with acute non-traumatic weakness may lead to timely intubation. 19Similarly, the detection of early signs of intracranial hypertension in a patient with severe  Emergency neurological life support bibliometrics Ramos et al.
traumatic brain injury would possibly prevent brain herniation. 20By recognizing the importance of this fast workup, health professionals and institutions would probably increase their interest in ENLS certification and training.In the current study, "Intracranial Hypertension and Herniation" (►Table 5) was the ENLS module with the greatest impact.This is one of the most basic and general modules, since various brain pathologies may lead ultimately to intracranial hypertension and brain herniation.
Even with the overt importance of a proper systematic and concise approach for neurologic emergencies, the demand for certification on ENLS is still limited when compared with its analogs in trauma and advanced cardiovascular support (ATLS and ACLS, respectively).This fact may find an explanation in the time of activity of each program.The ATLS was introduced in 1980 3 and has now been taught to more than 1 million physicians in more than 80 countries worldwide (data retrieved from facs.org/quality-programs/trauma/education/advanced-traumalife-support/ in December 2022). 3Likewise, the ACLS was presented in the middle 70s as the result of the second National Conference held on cardiopulmonary resuscitation (CPR) and emergency cardiac care (ECC) in 1973, which recommended delivery of advanced cardiac life support by trained personnel be required of all life-support units and hospitals on an integrated, community-wide basis and that training in CPR and techniques of ECC be under standards set by the AHA. 21,22Every year, the ACLS course is cumulatively accessed throughout the world by over 1.3 million candidates. 22As ENLS consolidates over the following years in different localities, advocacy efforts and community engagement seem to be the most promising way to foretaste acute neurological care, as done by ATLS and ACLS.
The accessibility of ENLS protocols may indeed influence their adoption and utilization in the scientific and medical communities.The protocols, devised by the Neurocritical Care Society, are not widely and freely available but rather necessitate a purchase.This financial barrier could potentially limit the dissemination and implementation of ENLS, particularly in low-and middle-income countries or among individual practitioners and smaller healthcare establishments with restricted budget allocations for accessing scientific materials.It is plausible that this financial aspect could subsequently influence the number of research articles discussing or utilizing ENLS, as the researchers might prefer or be constrained to utilize freely accessible guidelines and protocols.Thus, while ENLS provides a structured and standardized approach toward managing neurological emergencies, its broader impact on clinical practices and research might be restrained by its limited accessibility.Future initiatives or collaborations that facilitate wider, cost-effective access to these protocols might enhance their reach and implementation globally, fostering further research and potentially elevating patient care standards in neurological emergencies.
In the authors' opinion, the repercussions of ENLS on scientific literature are still low.The majority of papers only mentioned ENLS in the references section (►Figure 4).When excluding ENLS official publications, only 65 articles mentioned ENLS in the title, abstract, keywords, or text.The ENLS protocols are being updated constantly and the number of certified professionals is increasing.However, only 34 institutions in the USA and 9 in other countries require ENLS certification for some or all of their students and/or care providers (data retrieved from https://enls.neurocriticalcare.org/about/enls-institutions in December 2022).In addition, live ENLS courses have been held in 35 countries (data retrieved from https://enls.neurocriticalcare.org/about/statistics in December 2022).Therefore, there is still much to be done to ensure ENLS dissemination and that more institutions recognize the importance of this certification.

Limitations
The present bibliometric study has some limitations.First, only one database (Elsevier's Scopus) was used.However, this is one of the most comprehensive databases that track citation patterns, including over 71.2 million records post-1969 with reference. 23The decision to utilize Scopus exclusively was also influenced by its comprehensive inclusion of databases such as Medline and Embase, as well as its provision of reliable citation count data, crucial for executing robust bibliometric analyses.It's noteworthy that other databases like Lilacs and Scielo, while being significant, do not offer citation count data, and Google Scholar, which encompasses a wide range of internet references, was not chosen to ensure the impact assessment remained strictly within the bounds of scientific literature.Second, we considered only the country and its respective region and income category based on the corresponding author's affiliation.These affiliations may differ from other authors who also contributed to the studies.Third, recent articles did not have the same time exposure when compared with older articles, certainly affecting the total number of citations.Therefore, we also analyzed the number of citations per year per article, which helps to minimize these discrepancies.Fourth, only English-language articles were included.Articles published in other languages would possibly impact our findings.Fifth, we evaluated the repercussions of ENLS only on the scientific literature.
In conclusion, we found that the ENLS repercussion on the scientific literature is low, although increasing.The majority of papers that mentioned ENLS were secondary research and were mainly published by authors from high-income countries.Most articles only mentioned ENLS in the references section.Usually, the health professionals responsible for the initial management of neurocritically ill patients are not specialists in neurocritical care, who are frequently contacted after the first measures.Therefore, not only neurocritical care specialists but also all professionals who are likely to be exposed to scenarios of neurological emergencies should receive ENLS training.To increase the ENLS repercussion and training, some measures might be useful.We suggest making ENLS training a requirement for emergency department and intensive care professionals; making ENLS Emergency neurological life support bibliometrics Ramos et al. 9 available in several languages, and adding regional particularities to the protocols with partnerships with local medical societies.

Figure 1
Figure 1 Longitudinal pattern of publications mentioning Emergency Neurological Life Support from 2012 to 2021.

Figure 2
Figure 2 Correlation between the number of articles mentioning Emergency Neurological Life Support (ENLS) with the 5-year Impact Factors of destiny journals.Each small circle indicates a separate journal.Only journals with five or more articles were considered.ENLS protocols were excluded from the analysis.

Figure 3
Figure 3 (A) Mean number of citations per article according to country income of articles mentioning Emergency Neurological Life Support (ENLS).Only citations up to 2021 were computed (N ¼ 392 articles).(B) Mean number of citations per year per article according to country income of articles mentioning ENLS.Only citations up to 2021 were computed (N ¼ 392 articles).(C) Mean 5-year destiny journal impact factor according to country income of articles mentioning ENLS.Data in A and B utilize complete years up to 2021 for analysis; discrepancies in article counts may be due to additional reports retrieved up to the search date in 2022.

Figure 4
Figure 4 Section of appearance of Emergency Neurological Life Support in the included articles.

Table 1
The ten articles mentioning the Emergency neurological life support with the highest number of citations year IF.There was no correlation between the number of articles and 5-year IF (►Figure 2).Arquivos de Neuro-Psiquiatria Vol.82 No. 1/2024 © 2024.The Author(s).Emergency neurological life support bibliometrics Ramos et al. 3 Country, region, and income category ►Table 3 presents the most prominent countries, regions, and income categories within ENLS research.Articles were published by authors from 41 different countries.The USA was, by far, the most prolific (53.92%;N ¼ 227/421 articles).

Table 2
Articles, citations, citations per article, and 5-year destiny journal impact factor analysis of publications mentioning the Emergency neurological life support stratified by journals.N ¼ 421 Ã Only citations up to 2021 were computed (N ¼ 392 articles).

Table 3
Articles, citations, citations per year, and 5-year destiny journal impact factor analysis of publications mentioning the Emergency neurological life support (ENLS) research stratified by 15 countries with highest number of publications in the field, by world region and by country income.N ¼ 421

Table 4
Articles, citations, citations per article, and 5-year destiny journal impact factor analysis of publications mentioning the Emergency neurological life support (ENLS) stratified by research type and subtype.N ¼ 421 Abbreviations: ENLS, Emergency Neurological Life Support.IF, Impact Factor.Note: Ã Only citations up to 2021 were computed (N ¼ 392 articles).

Table 5
Emergency neurological life support modules and their mean number of citations per article and mean number of citations per year per article Arquivos de Neuro-Psiquiatria Vol.82 No. 1/2024 © 2024.The Author(s).